Spatio-temporal distribution of malaria vectors (Diptera: Culicidae) across different climatic zones of Iran

Transcription

1 498 Asian Pacific Journal of Tropical Medicine (2011) Contents lists available at ScienceDirect Asian Pacific Journal of Tropical Medicine journal homepage: Document heading doi: Spatio-temporal distribution of malaria vectors (Diptera: Culicidae) across different climatic zones of Iran Ahmad Ali Hanafi-Bojd 1*, Shahyad Azari-Hamidian 2, Hassan Vatandoost 1, Zabihollah Charrahy 3 1 Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 2 School of Health, Guilan University of Medical Sciences, Rasht, Iran 3 Department of Education, Jehad-e-Daneshgahi of Tehran University, Tehran, Iran ARTICLE INFO Article history: Received 12 January 2011 Received in revised form 11 March 2011 Accepted 15 May 2011 Available online 20 June 2011 Keywords: Anopheles Malaria Distribution GIS Iran ABSTRACT Malaria is a main vector-borne public health problem in Iran. The last studies on Iranian mosquitoes show 31 Anopheles species including different sibling species and genotypes, eight of them are reported to play role in malaria transmission. The objective of this study is to provide a reference for malaria vectors of Iran and to map their spatial and temporal distribution in different climatic zones. Shape files of administrative boundaries and climates of Iran were provided by National Cartographic Center. Data on distribution and seasonal activity of malaria vectors were obtained from different sources and a databank in district level was created in Excel 2003, inserted to the shape files and analyzed by ArcGIS 9.2 to provide the maps. Anopheles culicifacies Giles s.l., Anopheles dthali Patton, Anopheles fluviatilis James s.l., Anopheles maculipennis Meigen s.l., Anopheles sacharovi Favre, Anopheles stephensi Liston, and Anopheles superpictus Grassi have been introduced as primary and secondary malaria vectors and Anopheles pulcherrimus Theobald as a suspected vector in Iran. Temporal distribution of anopheline mosquitoes is restricted to April-December in northern Iran, however mosquitoes can be found during the year in southern region. Spatial distribution of malaria vectors is different based on species, thus six of them (except for Anopheles maculipennis s.l. and Anopheles sacharovi) are reported from endemic malarious area in southern and southeastern areas of Iran. The climate of this part is usually warm and humid, which makes it favorable for mosquito rearing and malaria transmission. Correlation between climate conditions and vector distribution can help to predict the potential range of activity for each species and preparedness for malaria epidemics. 1. Introduction Malaria is one of the most important communicable diseases transmitted by anopheline mosquitoes (Diptera: Culicidae) to humans. This disease is endemic in 108 countries around the world. In 2008, there were an estimated 243 million cases of malaria causing deaths, mostly of children under 5 years old[1]. It is one of the most infectious diseases in Iran with an average of about annual cases in the last decade, while total recorded cases has dropped to about in 2010 (Ministry of Health, annual reports). More than 80% of malaria cases in Iran are reported from three provinces of Sistan *Corresponding author: Hanafi-Bojd AA, Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran, P.O. Box: Fax: aahanafibojd@tums.ac.ir and Baluchistan, Hormozgan, and Kerman in southern and southeastern areas of the country[2]. There is another focus of the disease in northwestern Iran with an epidemic in recent years[3]. The most routes of malaria cases are immigration from Afghanistan and Pakistan to southern and southeastern areas of the country, as well as the Azerbaijan Republic in the northwest. The first study on malaria vectors was conducted about 90 years ago, when Latishev in 1921 identified Anopheles maculipennis Meigen s.l. (An. maculipennis) as the vector of malaria in northern areas of the country[2]. The genus Anopheles Meigen includes seven subgenera and at least 463 species and more than 50 unnamed members of species complexes[4]. About 70 species of them are malaria vectors in which about 40 are more important[5]. So far 31 species of the genus Anopheles representing two subgenera (Anopheles and Cellia), including different sibling species and genotypes, are recorded in the country, 16 out of them are in complexes or sibling species that some

2 Ahmad Ali Hanafi-Bojd et al./asian Pacific Journal of Tropical Medicine (2011) of them introduced as malaria vectors[6-9]. In southern areas of the country, Anopheles culicifacies (An. culicifacies) Giles s.l., Anopheles dthali (An. dthali) Patton, Anopheles fluviatilis (An. fluviatilis) James s.l., Anopheles stephensi (An. stephensi) Liston and Anopheles superpictus (An. superpictus) Grassi are known to be proven malaria vectors, while there is also report of sporozoite infection of Anopheles pulcherrimus (An. pulcherrimus) Theobald in southeastern Iran[2,10-12]. Also An. maculipennis s.l., Anopheles sacharovi (An. sacharovi) Favre and An. superpictus are introduced as malaria vectors of western, northwestern and central plateau[2,11]. Recently, a study reported Anopheles hyrcanus (An. hyrcanus) Pallas (infected to Plasmodium falciparum in Guilan Province, northern Iran, by nested polymerase chain reaction assay[13], but more studies are needed to confirm this species as malaria vector in Iran. Anopheles hyrcanus Group needs to be studied extensively in the western Palaearctic Region including Iran[14]. Figure 1 shows the map of Iran. It has a variable climate affected by heat, humidity and clouds, rainfall, wind and dust, radiation and thunder, respectively. Based on these six factors, fifteen climatic zones including Southern boundary zone(1), Caspian hinterland area(2), Central Iran area(3), Azeri area(4), Khuzy area(5), Moghani area(6), estern Zagros region(7), Eastern Zagros region(8), Caspian littoral area(9), South hinterland area(10), Large Sistani area(11), Baluchi area(12), Makoui area(13), Small Sistani area(14), and High Zagros area(15) have been described[15](figure 2). Also another (modified) classification demonstrates seven microclimates including: Arid (A), absolutely arid (AA), highly semi-arid (HAS), moderate semi-arid (MSA), slight semi-arid (SSA), semi-wet (S) and wet () (Figure 2). Each climate provides favorite conditions for some Anopheles species. Average temperature in arid area is and annual rainfall is mm (Figure 2). Absolute Arid climate has average temperature and rainfall of and mm, respectively (Figure 2). Highly semi-arid climate contains areas with an average temperature of 7-10 and annual rainfall of mm. In moderate semiarid climate, average temperature and annual rainfall are and mm. Slight semi-arid climate covers areas with an average temperature of 7-10 and annual rainfall of mm (Figure 2). Semi-wet climate is mainly located in average temperature of 7-10 and annual rainfall of mm. Finally, the et climate has an average temperature of 0-10 and annual rainfall of mm. Therefore in the northwest of Iran, winters are cold with heavy snowfall and subfreezing temperatures during December and January. Spring and fall are relatively mild, while summers are dry and hot. In the south, winters are mild and summers are very hot, having average daily temperatures in July exceeding 38. On the Khuzestan plain, summer heat is accompanied by high humidity. In general, Iran has an arid climate in which most of the relatively scant annual precipitation falls from October through April. In most of the country, yearly precipitation averages 250 mm or less. The major exceptions are the higher mountain valleys of the Zagros and the Caspian coastal plain, where precipitation averages at least 500 mm annually. In the western part of the Caspian, rainfall exceeds mm annually and is distributed relatively evenly throughout the year. This contrasts with some basins of central plateau that receive 100 mm or less of precipitation annually (Figure 2). Figure 1. Map of Iran. Micro-climates <all other values> A A.A H.S.A M.S.A S.S.A S. Rainfall Temperature N S E Climates Temperature Micro-climtes Rainfall Figure 2. Climatic zones, microclimates, temperature and rainfall thematic maps of Iran. The aim of the present study is to map the spatial distribution of main malaria vectors in different counties of Iran based on the reports of the previous studies, and to match it with different climatic variables and areas. Also in different climates, the spatial distribution of one Anopheles species may be affected by some factors such as preferred host accessibility, human activity, etc. The last shape files of administrative boundaries (including 31 provinces), thematic maps of rainfall and temperature, and also map of climates of Iran were obtained from the National Cartographic Center. A databank for distribution of malaria vectors was created in Excel software (Microsoft 2003) and then used for preparing the distribution maps in ArcGIS 9.2 software. These data were prepared and analyzed by ArcMap for spatial distribution mapping of the main malaria vectors at the county level in different climates and their temporal activity through the year.

3 500 Ahmad Ali Hanafi-Bojd et al./asian Pacific Journal of Tropical Medicine (2011) Distribution of malaria vectors in different climatic zones of Iran There are 31 Anopheles species including different sibling species and genotypes in Iran, eight of them are assumed to play role as malaria vectors. The present investigation emphasizes on the distribution of seven proven and one suspected vectors that are distinguishable morphologically, because most of obtained data were based on morphological characters. Therefore sibling species as the results of molecular studies are not included in our mapping. In southern Iran from the west to the east, the weather is warm and humid and Anopheles species are active during the year (Figure 3). In other parts, the anopheline mosquitoes mainly start their activity during the spring, so that from June to October they can be found in all parts of their distribution range. After that from November temperature decreases in about 20 provinces, therefore in January minimum activity of Anophelinae can be observed (Figure 3). April May June-October November December January February March Figure 3. Temporal distribution of anopheline mosquitoes in Iran. An. (Cel.) culicifacies Giles s.l. is the main malaria vector of Sistan and Baluchistan Province in southeastern Iran[10]. This complex consists of two species A and B (or probably a new species)[8,16,17] and is mainly distributed in southern and southeastern areas of Iran[6,18]. An. culicifacies s.l. occurs mainly in Sistan and Baluchistan, Kerman and Hormozgan Provinces. This species was implicated as a vector of malaria in Iran during an epidemic at Zabol (Sistan) in 1959[19]. It is the main malaria vector in southeastern corner of the country[11]. In Baluchistan the main peak of activity of the species occurs in April-May, whereas the secondary peak fluctuated from August to November. Study in southeastern Iran found considerable numbers of An. culicifacies s.l. resting outdoors in caves and pit shelters, with more than 40% of female freshly blood-fed specimens, suggesting high proportion of exophagy. The majority of endophagic females remained indoors for several days until becoming gravid. Human Blood Index (HBI) of this species in Baluchistan is reported from 1.18% to 20%. Sporozoite rate for this species is reported from 1% from Bandar Abbas in Hormozgan Province to 4.7% in Zabol, Sistan and Baluchistan Province[19]. Rice fields of Baluchistan area during April-September are the main larval breeding sites of An. culicifacies s.l., along with irrigated palms and stream pools in other parts of its distribution area. During winter months, from October to April, stream pools serve as the predominant oviposition sites of this species in most areas[10,20]. The spatial distribution of this species is restricted to Bushehr, Hormozgan, Kerman, Sistan and Baluchistan, South Khorasan and Khuzistan Provinces. It mainly reported from moderate semi-arid and southern part of absolute arid climates (Figure 4)[6,8,10-12,18,21-27]. Legend <all other values> H.S.A S. M.S.A A S.S.A A.A An. culicifacies An. maculipennis An. dthali An. fluviatilis N E S Figure 4. Distribution maps of An. culicifacies s.l., An. dthali, An. fluviatilis s.l. and An. maculipennis s.l. in different climates of Iran. An. (Cel.) dthali Patton is a secondary vector of malaria in southern Iran especially in mountainous areas of Hormozgan Province[28-30]. It has been found in southern parts of the Zagros chain, and coastal area of the Persian Gulf up to m[29,30]. This species is widespread throughout the coastal and mountainous areas with high density in mountain areas. In these areas An. dthali is active throughout the year with two peaks, first in September-October and the other in April. This Anopheles is usually rests outdoors, although it is found in permanent human dwellings, tents, animal shelters, and food stores. Indoors, it has been collected from walls, and particularly from spider webs and hanging clothes. Outdoors, they are commonly found in natural shelters such as holes in river banks, rodent holes and old ruined Qanats. Precipitation tests on specimens from different parts showed up to 20.8% were positive for human blood. Anthropophilic index is varied between 1%-25% depend on locality. Sporozoite rates for An. dthali are reported from 0.67% to 2.08% in Iran. Larvae of this Anopheles were found in water with high salinity (2.7 parts per 1 000) in rural areas. An. dthali breeds in pebbly margins of rivers, springs, pits around springs with or without vegetation, pools in dried-up river beds, and palm irrigation canals in Hormozgan Province. In Bandar Abbas County, larvae were also found in mineral water. It is found in water with high salinity. The water temperature of breeding places ranging between 13 and 28, with a ph of An. dthali is reported mainly from southern part of absolute arid, and parts of moderate semi-arid, slight semi-arid and high semi-arid climates (Figure 4). It is reported from Bushehr, Chaharmahal and Bakhtiari, Fars, Hamedan, Hormozgan, Ilam, Isfahan, Kerman, Kermanshah, Khuzistan, Kohgiluye and Buyerahmad, Lorestan, Sistan and Baluchistan, and Yazd Provinces (Figure 4)[6,8,11,12,18,21-27,29-33]. An. (Cel.) fluviatilis James s.l. is introduced as a secondary vector in southern and southeastern areas of the country[11]. In An. fluviatilis complex the species T, U and V are reported based on rdna ITS2 and D3 sequence analysis in Iran[8,9], though Naddaf et al[34] were in doubt about the

4 Ahmad Ali Hanafi-Bojd et al./asian Pacific Journal of Tropical Medicine (2011) occurrence of the species V. This Anopheles is distributed on the southern slopes of the Zagros chain, from southwest of Kermanshah Province to Sistan and Baluchistan Province in the southeastern part of Iran, and found at altitude from 50 meter to meter. Its seasonal activity and maximum density has two periods, from April to June and from late September to December on plains and from the end of spring up to the beginning of autumn in foothill area. This species is reported both endophilic and exophilic, although in some areas it shows a marked exophilic tendency. Due to the outdoor sleeping habits of the local population in this area during warm months of spring and summer, this species is considered as exophagic. Human blood index of this species is reported from 2.68% to 28.6% in different ecological zones. Sporozoite rate for this Anopheles is recorded 1.4%- 11%. An. fluviatilis breeds in fresh, slow flowing or stagnant waters, vast marshes, river banks, pits in the beds of stony or sandy rivers and rainfall pits[35,36]. This species is reported from Bushehr, Fars, Hormozgan, Ilam, Kerman, Kermanshah, Khuzistan, Kohgiluye and Buyerahmad, Lorestan and Sistan and Baluchistan Provinces, where climates are moderate, slight or high semi-arid (Figure 4)[6,8, 11,12,18,21,23,24,31,35,37]. An. (Ano.) maculipennis complex comprises 7 species in Iran: Anopheles atroparvus van Thiel, Anopheles labranchiae Falleroni, An. maculipennis, Anopheles melanoon Hachett, Anopheles messeae Falleroni, Anopheles persiensis Linton, Sedaghat and Harbach, and An. sacharovi[6,8]. In the Maculipennis Group only An. sacharovi can be distinguished morphologically from others[38-40], thus most of published data introduced An. maculipennis s.l. and An. sacharovi as two species that are included in malaria transmission in northern and northwestern areas of the country[2,3,11] based on a morphological key[39]. An. maculipennis complex has been identified as the major vector of malaria in the Caspian Sea littoral. Edrissian et al[41] and Vatandoost et al[42] reported HBI of 4.9%-5% for An. maculipennis s.l. Sporozoite rate for this species is reported 0.33%. An. maculipennis s.l. has endophilic and endophagus behavior. Larval habitats are including clear samples along the edges of slowing rearends of water supply channel and roadside ditches, as well as rice fields. Its seasonal activity is mainly between late May to October with a peak in August[43]. There is no report of this species from Bushehr, Hormozgan, Kerman, Ilam, Sistan and Baluchistan, South Khorasan, Qom and Yazd Provinces (Figure 4). This Anopheles is mainly distributed in wet, slight semi-arid, moderate semi-arid and high semiarid climates, although there are reports of existence in absolute arid climate (Figure 4)[3,6,8,18,21,32,33,37,40,42,44-59]. An. (Cel.) pulcherrimus Theobald is reported serologically positive to Plasmodium falciparum and Plasmodium vivax in Sistan and Baluchistan Province and introduced as a suspected vector in that area[10,12]. Slow moving streams, ditches, rice fields, pools, marshes and other types of waters with or without vegetation have been reported as the breeding sites for An. pulcherrimus larvae. However, rice fields, weedy irrigation channels, marshes and any kind of clean stagnant water, overgrown with vegetation, but not too heavily shaded, have been reported as the most favorable sites[60]. The species had been active throughout the year with one peak of activity in August-September in Sistan and Baluchistan Province[10]. Human blood index of this species is reported 1.12%-9.9%, while its sporozoite rate was 3.5% in Qasre-qand, Sistan and Baluchistan Province[22,41]. This species is mostly exophilic, but a part of the population also uses indoor resting sites[60]. An. pulcherrimus occurs in moderate and highly semi-arid climates[15] (Figure 5) in Chaharmahal and Bakhtiari, Fars, Golestan, Hormozgan, Ilam, Kermanshah, Khuzistan, Kohgiluye and Buyerahmad, Mazandaran, North Khorasan, and Sistan and Baluchistan Provinces[8,11,12,18,22,23,31,37,58,60]. An. (Ano.) sacharovi Favre is a major vector of malaria in northwestern Iran and is distributed in foothills of Zagros Mountains from northwestern, western and southwestern areas of Iran, as well as northern belt. It is a member of An. maculipennis complex and only this species can be distinguished morphologically from other members of this complex in adult and larval stages[38,39]. This species is mainly endophilic and endophagus, although the relative exophilicity is also reported. Based on the survey of Yaghoobi-Ershadi et al[3] this species showed 38.5% blood fed on human alone and 23% on both human and dog in human dwellings, but the specimens that had fed on the animal shelters were negative for human blood. The anthropophilic index of An. sacharovi has been reported between 4.2% and 30.6% from Iran in 1969 but the sources of their blood meal smears were not stated[43]. Human blood index values of 26.5% from human dwellings and 9.4% from animal shelters were observed from East Azerbaijan and Khuzistan Provinces of Iran during [41]. Soporozoite rate for this Anopheles is reported 1%-2%[43]. Larval habitats include clear samples along the edges of the slowing rear-ends of water supply channel and roadside ditches, as well as rice fields. Seasonal activity starts from April and extends to October-November, with a peak in July-August in southern Iran, while in the northwest of the country it is active from late June to late November with one peak in late August[3]. This species is reported mainly from wet, moderate semi-arid and high semi-arid climates in Ardebil, East Azerbaijan, Fars, Guilan, Golestan, Kermanshah, Khuzistan, Kohgiluye and Boyerahmad, Kurdistan, Lorestan, Mazandaran, Qazvin, Tehran, and est Azerbaijan Provinces (Figure 5)[3,6,8,11,21,37,38,42-46,50,55,57,61,62]. Legend <all other values> H.S.A S. M.S.A A S.S.A A.A N E An. Pulicherrimus An. superpictus An. sacharovi An. stephenst S Figure 5. Distribution of An. pulcherrimus, An. sacharovi, An. stephensi and An. superpictus in different climates of Iran. An. (Cel.) stephensi Liston is the main malaria vector in southern coastal areas of Iran[2,11,63]. The species includes three egg phenotypes: mysorensis, typical and intermediate, all exist in Iran[7]. These egg phenotypes are natural

5 502 Ahmad Ali Hanafi-Bojd et al./asian Pacific Journal of Tropical Medicine (2011) variations and systematically considered infrasubspecific forms of the species[8,24]. The previous investigations have shown it to be the most prevalent anopheline species in the malarious area of southern Iran up to altitude of 900 m[64], although recent studies extended its distribution up to m in Lorestan Province[32]. An. stephensi is active during the year in southern coastal area, with two peaks in April- May and September-October. It can be found from April to November in cold mountainous area with one peak of activity in July. This species is endophagous and endophilic. There are different reports of anthropophily for this species and HBI is recorded 0.5%-3.6% in different counties. Sporozoite rate of samples from the southern areas of Iran was reported from 0.2% to 1.8%. An. stephensi breeds in a wide range of both urban and rural habitats throughout its distribution region. In urban areas this species breeds in all sorts of water bodies, such as wells, cisterns, fountains, ornamental ponds, and in water used for building construction. Larvae can be collected from ponds, pools, stream margins, catch basins, and seepage canals. It is found in water with high salinity, sometimes reaching or even exceeding that of seawater. In rural areas, the breeding places are pools, streambeds, palm irrigation canals, at the margin of streams and rivers, seepages, and marshy areas with a gentle water flow[64,65]. This species is distributed mainly in moderate semi-arid and absolute arid climates, although high semiarid and slight semi-arid climates are also included. This species is reported from Bushehr, Fars, Hormozgan, Ilam, Kerman, Kermanshah, Khuzistan, Kohgiluye and Buyerahmad, Lorestan, Sistan and Baluchistan Provinces (Figure 5)[6-8,11,12,18,21-24,31,32,37,43,64,66]. An. (Cel.) superpictus Grassi is considered as a major malaria vector in central plateau, and the secondary one in the southern areas of the country[2,11]. Oshaghi et al[67] reported two distinct morphological forms (A and B) of this species from Iran, while molecular analysis of mitochondrial DNA COI-COII region separated this Anopheles into at least three genotypes X, Y and Z[68]. An. superpictus has a widespread distribution in Iran across the all climatic zones, from 50 to meter. It is reported from absolutely arid to wet climates (Figure 5). It is active during April to November is the most parts of the country with one peak in August-September. It is exophagic with both exophilic and endophilic behavior. Human blood index and sporozoite rates for this Anopheles are 11.4% and 0.65%-4.7%, respectively. Larvae of An. superpictus can be found in different water bodies with ground origin, especially sandy larval habitats of riverbeds with clear water. The species is recorded in all provinces of the country, however there is no formal report of it from Qazvin Province[3,6,8,11,12,18,21,23,31-33,37,41,42,44,46,47,49,50,53-55,57,58,67-70]. According to the present investigation, An. superpictus is found in almost all Iranian climates and that may explain why the species is collected from all areas of the country (Figure 5). This makes the species an important malaria vector in Iran especially in central plateau. An. culicifacies s.l., An. fluviatilis s.l., An. pulcherrimus and An. stephensi are found in 5-6 (out of 15) climates based on Masoodian s[15] classification or 2-4 climatic zones based on modified classification. These species are not collected from central and northern Iran except for An. pulcherrimus (Figure 4,5). There is an exceptional distributional focus of An. pulcherrimus in northeastern Iran (Figure 5). This is interesting in view of its occurrence in Middle Asia[58]. Also, An. dthali is not recorded in central and northern Iran, though it is found in 9 (out of 15) of Masoodian s climatic zones[15] and 4 (out of 7) modified classification (Figure 4). The general distributions of An. dthali, An. fluviatilis s.l., and An. stephensi seem to be similar in southern Iran (Figure 4,5) where they are the main and secondary vectors of malaria. However the distribution of An. culicifacies s.l. mostly occurs in the southeastern wards of the country (Figure 4) where it is known the main vector. An. maculipennis Group occurs in different climatic zones, 9 (out of 15) of Masoodian s climatic zones[15] and 5 (out of 7) modified classification for An. maculipennis s.l. and 8 (out of 15) and 3 (out of 7) for An. sacharovi respectively, and the group has a wide distribution in central, northern, western, and even southwestern Iran, however it does not occur in southeastern Iran and the southern part of the country (Figure 4,5). This is the reason An. maculipennis s.l. and An. sacharovi do not play role in malaria transmission in the main malaria foci in southern and southeastern Iran, however they are the main vectors in northern foci. Exact distribution of all members of the group is not clear because of problematic morphological identification of them. Although some species are found in similar climatic zones, they show different distribution or vice versa. The reason may be explained that the climatic zones are described here mostly based on temperature and rainfall and other environmental and biological features which influence distribution and abundance of mosquitoes such as altitude, water salinity influenced by soil texture and structure, larval habitat characteristics, plants, preferred hosts and so on need to be investigated more to answer the questions. Also, what we find out about the distribution of the species today has been critically influenced by human activities and climate change especially in recent decades. Using climatic data and ecological information about favorite conditions for breeding of different malaria vectors, GIS may predict the probable distribution areas of each species. This action needs a database consisting of ecological parameters which are suitable for breeding and survival of anopheline vectors of malaria. Although study on the fauna, biology, ecology, susceptibility status to insecticides and molecular taxonomy of Anopheles mosquitoes has an old history and information about anopheline mosquitoes in Iran has been collected during about 90 years, GIS-based studies are rare. This method can help entomologists to work more careful and will facilitate decision making for malaria control programs. Global warming can significantly impact on the distribution and severity of malaria on a global level, especially as a mosquito-borne disease which is highly sensitive to changes in climate. So developing models for distribution of Anopheles species based on environmental conditions and ecology of vectors will help us to have upto-date maps for each species. More studies are needed to create a well described database on biology, ecology, systematics and susceptibility status of malaria vectors at larval and adult stages in Iran. e recommend collecting such information from other vector-borne disease in the country for preparedness and early warning for probable epidemics especially in the natural disasters for implementation of any vector control measures.

6 Ahmad Ali Hanafi-Bojd et al./asian Pacific Journal of Tropical Medicine (2011) Conflict of interest statement e declare that we have no conflict of interest. Acknowledgements The authors are grateful to the personnel of the library of the School of Public Health, Tehran University of Medical Sciences, especially Mr. Davoodi for their kind assistance in providing some references. This study received no financial support. References [1] orld Health Organization. orld malaria report Geneva: HO. [Online] Available at: malaria_report_2009/en/index.html. [2] Edrissian GhH. Malaria in Iran, past and present situation. Iran J Parasitol 2006; 1(1): [3] Yaghoobi-Ershadi MR, Namazi J, Piazak N. Bionomics of Anopheles sacharovi in Ardebil Province, northwestern Iran during a larval control program. Acta Trop 2001; 78: [4] Harbach RE onwards. Mosquito Taxonomic Inventory. [Online]Available at: [Accessed on 17 December 2010]. [5] Service M. Mosquitoes (Culicidae). In: Lane RP, Crosskey R, editors. Medical insects and arachnids. London: Chapman and Hall; 1993, p [6] Sedaghat MM, Harbach RE. An annotated checklist of the Anopheles mosquitoes (Diptera: Culicidae) in Iran. J Vec Ecol 2005; 30: [7] Oshaghi MA, Yaghoobi F, Vatandoost H, Abaei MR, Akbarzadeh K. Anopheles stephensi biological forms, geographical distribution and malaria transmission in malarious regions of Iran, Pakistan. J Biol Sci 2006; 9(2): [8] Azari-Hamidian S. Checklist of Iranian mosquitoes (Diptera: Culicidae). J Vec Ecol 2007; 32(2): [9] Mehravaran A, Oshaghi MA, Vatandoost H, Abai MR, Ebrahimzadeh A, Roodi AM, et al. First report on Anopheles fluviatilis U in southeastern Iran. Acta Trop 2011; 117(2): [10] Zaim M, Subbarao SK, Manouchehri AV, Cochrane AH. Role of Anopheles culicifacies and An. pulcherrimus in malaria transmission in Ghassreghand (Baluchistan), Iran. J Am Mosq Control Assoc 1993; 9(1): [11] Manouchehri AV, Zaim M, Emadi AM. A review of malaria in Iran, J Am Mosq Control Assoc 1992; 8: [12] Ghavami MB, Zaim M, Javadjan E, Edrissian GhH, Nateghpoor M, Kanani A, et al. Anopheline sporosoite infection rate in Ghassreghand, Baluchistan, Iran (1995). Iran J Publ Health 1997; 26(3-4): [13] Djadid ND, Jazayeri H, Gholizadeh S, Rad ShP, Zakeri S. First record of a new member of Anopheles hyrcanus group from Iran: molecular identification, diagnosis, phylogeny, status of kdr resistance and Plasmodium infection. J Med Entomol 2009; 46(5): [14] Azari-Hamidian S, Abai MR, Ladonni H, Vatandoost H, Akbarzadeh K. Anopheles peditaeniatus (Leicester) new to the Iranian mosquito fauna with notes on Anopheles hyrcanus group in Iran. J Am Mosq Control Assoc 2006; 22(1): [15] Masoodian A. Climatic regions of Iran. J Geography & Dev 2003; 1(2): (In Persian with English abstract). [16] Zaim M, Javaherian Z. Occurrence of Anopheles culicifacies species A in Iran. J Am Mosq Control Assoc 1991; 7(2): [17] Oshaghi MA, Taghilo B, Moradi MT, Vatandoost H. Mosquitoes of Anopheles culicifacies complex, species A and B in Baluchistan using mtdna PCR- RFLP assay: the first report of species B from Iran. Hakim Res J 2004; 7: (In Persian with English abstract). [18] Saebi ME. Morphological study on anopheline larvae and their distribution in Iran [PhD dissertation]. Tehran, Iran: School of Public Health, Tehran University of Medical Sciences; 1987.(In Persian). [19] Manouchehri AV, Ghiassedin M. Annual report. Reports of the institute of parasitology and malariology, 1959; Publication No. 669, Tehran (In Persian). [20] Zaim M, Manouchehri AV, Motabar M, Emadi AM, Nazari M, Pakdad K, et al. Anopheles culicifacies in Baluchistan, Iran. Med Vet Entomol 1995; 9: [21] Manouchehri AV. A review on the ecology of malaria vectors in Iran. Publications of School of Public Health, Tehran University of Medical Sciences, 1985; No.77, Tehran (In Persian). [22] Mowlaii G, Zaim M, Manouchehri AV, Motabar M, Edrissian GhH, Ladonni H, et al. Biting behaviour of anopheline mosquitoes in Baluchistan, Iran. Iran. J Publ Health 1991; 20(1-4): [23] Kamyabi F, Mahmoudi E, Kouhestani Z. Determination of fauna and seasonal activity of Anopheles mosquitoes in Markazi region of Jiroft District. J Shahid Sadoughi Univ Med Sci 2002; 9(4): (In Persian with English abstract). [24] Azari-Hamidian S, Linton YM, Abai MR, Ladonni H, Oshaghi MA, Hanafi-Bojd AA, et al. Mosquito (Diptera: Culicidae) fauna of the Iranian islands in the Persian Gulf. J Nat Hist 2010; 44(15): [25] Macan TT, Leeson HS, Lumsden HR, Yofe J. Anopheles and malaria in the Near East. Mem Lond Sch Hyg Trop Med 1950; 7: [26] Dow RP. Notes on Iranian mosquitoes. Am J Trop Med Hyg 1953; 2: [27] Mofidi S. Distribution of the anopheline of Iran. Reports of the Institute of Parasitology and Malariology, 1953; Publication No. 225, Tehran (In Persian). [28] Manouchehri AV, Ghiasseddin M, Shaghudian ER. Anopheles dthali Patton, 1905, a new secondary vector in southern Iran. Ann Trop Med Parasit 1972; 66(4): [29] Vatandoost H, Shahi M, Hanafi-Bojd AA, Abai MR, Oshaghi MA, Rafii F. Ecology of Anopheles dthali Patton in Bandar Abbas District, Hormozgan Province, Southern Iran. Iran. J Arthropod- Borne Dis 2007; 1(1): [30] Manouchehri AV, Rohani F. Notes on the ecology of Anopheles dthali Patton in Southern Iran. Ann Trop Med Parasit 1975; 69(3): [31] Yaghoobi-Ershadi MR, Zaim M, Manouchehri AV. Studies on the biology of the mosquitoes in the district of Minab, Hormozgan Province, Iran, ( )1-Characteristcs of the larval breeding sites. J Environ Stud 1986; 13: (In Persian with English abstract). [32] Amani H. Study on fauna and characteristics of breeding places of malaria vectors, and reasons of remaining malaria focus in Aligoodarz District. [MSPH dissertation]. Tehran, Iran: School of Public Health, Tehran University of Medical Sciences; (In Persian). [33] Salehi-Shahraki F, Seyedi-Rashti MA. Study on malaria vectors and two new records in Farsan County, Chaharmahal-Bakhtiari Province. Shahrekord Univ Med Sci J 1998; 2(2): (In Persian with English abstract). [34] Naddaf SR, Razavi MR, Bahrami G. Molecular variation and distribution of Anopheles fluviatilis (Diptera: Culicidae) complex in Iran. Korean J Parasitol 2010; 48(3): [35] Eshghi N, Motabar M, Javadian E, Manouchehri AV. Biological

7 504 Ahmad Ali Hanafi-Bojd et al./asian Pacific Journal of Tropical Medicine (2011) features of Anopheles fluviatilis and its role in the transmission of malaria in Iran. Trop Geog Med 1976; 28: [36] Basseri HR, Moosakazemi SH, Yosefi S, Mohebali M, Hajaran H, Jedari M. Anthropophily of malaria vectors in Kahnouj District, south of Kerman, Iran. Iran J Publ Health 2005; 34(2): [37] Javadian E. Malaria situation of Khuzistan Province. Reports of the Institute of Parasitology and Malariology, 1971; Publication No. 1836, Tehran (In Persian). [38] Doosti S, Azari-Hamidian S, Vatandoost H, Oshaghi MA, Hosseini M. Taxonomic differentiation of Anopheles sacharovi and and An. maculipennis s.l. (Diptera: Culicidae) larvae by seta 2 (Antepalmate hair). Acta Med Iran 2006; 44(1): [39] Azari-Hamidian S, Harbach RE. Keys to the adult females and fourth-instar larvae of the mosquitoes of Iran (Diptera: Culicidae). Zootaxa 2009; 2078: [40] Sedaghat MM, Linton YM, Oshaghi MA, Vatandoost H, Harbach RE. The Anopheles maculipennis complex (Diptera: Culicidae) in Iran: molecular characterization and recognition of a new species. Bull Entomol Res 2003; 93: [41] Edrissian GhH, Manouchehri AV, Hafizi A. Application of an enzyme-linked immunosorbent assay (ELISA) for determination of human blood index in anopheline mosquitoes collected in Iran. J Am Mosq Control Assoc 1985; 1(3): [42] Vatandoost H, Abdoljabari Boonab R, Abai MR, Oshaghi MA, Rassi Y, Gholizadeh S, et al. Entomological survey in Kalibar, a resurgent malaria focus in East-Azerbaijan, Iran. Pakistan J Biol Sci 2005; 8(10): [43] Faghih MA. Malariology and malaria eradication. Tehran: Tehran University Press; 1969 (In Persian). [44] Mesghali A. Detailed report on the distribution of mosquitoes of the genus Anopheles in Iran. Reports of the Institute of Parasitology and Malarialogy, 1961; Publication No. 844, Tehran (In Persian). [45] Zolotarev ER. Anopheles maculipennis of northern Iran. Med Parasitol Parasitic Dis 1945; 14: (In Russian). [46] Zaini A. Entomological survey and susceptibility status of Anopheline malaria vectors in East-Azerbijan, est-azerbijan and Kurdistan Provinces. Reports of the Institute of Parasitology and Malariology, 1971; Publication No. 1846, Tehran (In Persian). [47] Zaim M. The mosquito fauna of Kashan, public health importance and control. Desert Sci Res 1987; 18: 1-14 (In Persian with English abstract). [48] Zaim M, Karami M, Edalat H. Fauna, distribution and night biting activity of Culicidae in Amol district (Caspian Sea littoral), Iran (1994). Prague, Czech Republic: IX SOVE European Meeting; 1995, p: [49] MirHashemi M. Study on fauna and breeding places of Culicidae mosquitoes of Mashhad County. [MSPH dissertation]. Tehran, Iran: School of Public Health, Tehran University of Medical Sciences; (In Persian). [50] Vahabi A. Fauna and distribution of Anophelinae (Diptera: Culicidae) mosquitoes of Kordestan Province in J Kordestan Univ Med Sci 2001; 6(21): (In Persian with English abstract). [51] Azari-Hamidian S, Joeafshani MA, Mosslem M, Rassaei AR. Adult mosquito habitats and resting-places in Guilan Province (Diptera: Culicidae). Hakim Res J 2003; 6(3): (In Persian with English abstract). [52] Oshaghi MA, Sedaghat MM, Vatandoost H. Molecular characterization of the Anopheles maculipennis complex in the Islamic Republic of Iran. East Mediterr Health J 2003; 9(4): [53] Azari-Hamidian S, Joeafshani MA, Rassaei AR, Mosslem M, Moussavi-Eivanaki E. Mosquito fauna of the genus Anopheles (Diptera: Culicidae) in Guilan Province. Modarres J Med Sci 2004; 6(2): (In Persian with English abstract). [54] Ghavami MB, Ladonni H. Fauna and frequency of mosquitoes (Diptera: Culicidae) in Zanjan Province, Zanjan Univ Med Sci J 2006; 13(53): (In Persian with English Abstract). [55] Abai MR, Azari-Hamidian S, Ladonni H, Hakimi M, Mashhadi- Esmail K, Sheikhzadeh K, et al. Fauna and checklist of mosquitoes (Diptera: Culicidae) of East Azerbaijan Province, northwestern Iran. Iran J Arthropod-Borne Dis 2007; 1(2): [56] Djadid ND, Gholizadeh S, Tafsiri E, Romi R, Gordeev M, Zakeri S. Molecular identification of Palearctic members of Anopheles maculipennis in northern Iran. Malaria J 2007; 6: [57] Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Linton YM, et al. Distribution and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Med Vet Entomol 2009; 23: [58] Azari-Hamidian S, Abai MR, Arzamani K, Bakhshi H, Karami H, Ladonni H, et al. Mosquitoes (Diptera: Culicidae) of North Khorasan Province, northeastern Iran and the zoogeographic affinities of the Iranian and Middle Asian mosquito fauna. J Entomol 2011; 8(3): [59] Gutsevich AV. On the mosquitoes of north Iran. Compt Rend Acad Sci USSR 1943; 40: (In Russian). [60] Zaim M, Manouchehri AV, Motabar M, Mowlaii G, Kayedi MH, Pakdad K, et al. Ecology of Anopheles pulcherrimus in Baluchistan, Iran. J Am Mosq Control Assoc 1992; 8(3): [61] Etherington D, Sellick G. Notes on the bionomics of Anopheles sacharovi in Persia and Iraq. Bull Entomol Res 1946; 37: [62] Sedaghat MM, Linton YM, Nicolescu G, Smith L, Koliopoul G, Thanassius KZ, et al. Morphological and molecular characterization Anopheles (Anopheles) sacharovi Favre, a primary vector of malaria in the Middle East. Syst Ent 2003; 28(2): [63] Vatandoost H, Oshaghi MA, Abai MR, Shahi M, Yaghoobi F, Baghaii M, Hanafi-Bojd AA, et al. Bionomics of Anopheles stephensi Liston in the malarious area of Hormozgan Province, southern Iran. Acta Trop 2006; 97(2): [64] Manouchehri AV, Javadian E, Eshghi N, Motabar M. Ecology of Anopheles stephensi Liston in southern Iran. Trop Geog Med 1976; 28: [65] Vatandoost H, Shahi M, Abai MR, Hanafi-Bojd AA, Oshaghi MA, Zamani G. Larval habitats of main malaria vectors in Hormozgan Province and their susceptibility to different larvicides. Southeast Asian J Trop Med Publ Health 2004; 35: [66] Oshaghi MA, Yaaghoobi F, Abaie MR. Pattern of mitochondrial DNA variation between and within Anopheles stephensi (Diptera: Culicidae) biological forms suggests extensive gene flow. Acta Trop 2006; 99: [67] Oshaghi MA, Shemshad Kh, Yaghoobi-Ershadi MR, Pedramb M, Vatandoost H, Abaie MR, et al. Genetic structure of the malaria vector Anopheles superpictus in Iran using mitochondrial cytochrome oxidase (COI and COII) and morphologic markers: A new species complex? Acta Trop 2007; 101: [68] Oshaghi MA, Yaghoobi-Ershadi MR, Shemshad Kh, Pedram M, Amani H. The Anopheles superpictus complex: introduction of a new malaria vector complex in Iran. Bull Soc Pathol Exot 2008; 101: [69] Doroudgar A, Dehghani R, Hooshyar H, Sayyah M. Epidemiology of malaria in Kashan. J Med Fac Guilan Univ Med Sci 2000; 8(31-32): (In Persian with English abstract). [70] Hanafi-Bojd AA, Vatandoost H, Oshaghi MA, Haghdoost AA, Shahi M, Sedaghat MM, et al. Entomological and epidemiological attributes for malaria transmission and implementation of vector control in southern Iran. Acta Trop doi: / j.actatropica